The present study was conducted on twelve female bovines (buffalo=7 and cattle=5) presented to Teaching Veterinary Hospital of GADVASU with clinical signs suggestive of cardiac insufficiency. The clinical examination followed by ultrasonography revealed presence of single or multiple lung and/or liver cysts in these patients. The common clinical signs were brisket edema (n=9), brisket+limb edema (n=2), jugular engorgement (n=3), dyspnoea (n=6), abducted elbows (n=3) and fever (n=3). Upon ultrasonography, single and multiple cystic densities in hepatic tissue (n=10) & lung parenchyma (n=11) were observed. A significant finding was compression of the heart (n=8) due to multiple cysts in the lungs that lead to cardiac tamponade i.e. inability of heart to pump to its full capacity which may have advanced to clinical signs mimicking that of cardiac insufficiency. Present study reports ultrasonographic diagnosis of lung or liver cysts with occurrence of atypical signs like ventral edema, dyspnoea and jugular distension.
Cystic echinococcosis (CE) caused by the metacestode stage of Echinococcus granulosus is a cause of major public health concern worldwide. It is one of the important emerging and re-emerging parasitic zoonosis endemic in India, which affects a wide range of mammals (Cardona and Carmena, 2013). Carnivores (definitive host) carry the adult worms in the small intestine and intermediate larval stage (hydatid cyst) develops in the internal organs of various mammalian species. The intermediate hosts (human beings and ruminants) acquire the infection through ingestion of infected eggs (Eckert and Deplazes, 2004). The parasite has been recorded from the most food producing animals in the country (Pednekar et al., 2009). The infection leads to heavy economic losses due to the condemnation of infected offals, particularly liver and lungs and to lowered meat and milk production (Torgerson, 2003). The contributing factors to the higher incidence of hydatid disease in developing countries like India are presence of stray dogs, poor sanitary infrastructure, free access of dogs to slaughter waste, low public awareness and lack of strict meat inspection measures (Singh et al., 2012). In the food producing animals, the disease is mostly considered asymptomatic and the definitive diagnosis is usually made on slaughter or post mortem (Khan et al., 2010). Mostly the infected intermediate hosts may remain asymptomatic or may have signs and symptoms similar to the human disease (Schwabe, 1986). Ante-mortem diagnosis of lung and liver cysts is a serious problem, as till now no specific clinical signs have been identified. A recent report documented symptoms like coughing, dyspnoea and stridor in dairy cattle and buffaloes with cystic densities in the lung area (Chuadhari et al., 2017).
Detection of lung and liver cysts in live animals is very important as it may be useful in the assessment of disease severity and therefore such animals may be culled to prevent spread of this catastrophic zoonoses. Despite of all these factors, the clinical presentation of hydatid disease is poorly understood in bovine hosts. The current study will help veterinary practitioners in the better understanding of clinical signs associated with the disease and in the differential diagnosis where the clinical signs may mimic diseases of other organ systems.
Material and Methods
Animals, History and Physical Examination
The study included twelve sick bovine animals (buffalo-7; cattle-5) presented to the Teaching Veterinary Hospital, Guru Angad Dev Veterinary & Animal Sciences University with the clinical signs indicative of cardiac insufficiency. Suspecting some cardiac involvement, these animals were subjected to a comprehensive clinical examination and detailed history and clinical symptoms were recorded. Blood samples were collected for routine hemato-biochemical examination(s) to note down any changes associated with the disease.
Owing to the suspicion of some cardiac affection, detailed thoracic and abdominal ultrasonography was carried out. For ultrasonographic examination, animals were prepared by clipping hair from lung (5-12 ICS in shape of triangle, both sides) and liver (5-12 ICS, right side) region. The multi frequency convex transducer (3.5-5 MHz) with penetration depth of 30 cm was moved dorsoventrally at each intercostal space in standing animals using M-turbo portable ultrasound scanner (FUJIFILM SonoSite, Inc. USA). Detection of any cavitary lesion in the hepatic parenchyma (Fig. 1) or in lung region/ surface (Fig. 2) was used as a criterion in the detection of cyst. Cardiac ultrasound as described by Braun et al. (2001) was performed using 1-5 MHz sector cardiac probe to evaluate the cardiac functioning. The patients were prepared by shaving 25 x 25 cm area over the 3rd-5th ICS on both left and right side.
|Fig. 1: Ultrasonographic image showing three encapsulated thin walled cavitary lesions (C) in the hepatic parenchyma||Fig. 2: Ultrasonographic image showing three cystic lesions (C) on the lung surface|
Mean and standard error means for various parameters were calculated using the SAS software. The subjective parameters were compared using percentage
Results and Discussion
Physical Examination and Clinical Signs
The study included seven buffalo and five cattle that were presented with clinical symptoms suggestive of cardiac insufficiency. All the presented animals were adult females with mean age of 6.8±0.72 years (range 4-10 years). Similar to the observations in the present study higher prevalence of hydatid disease is observed in older animals (Salih et al., 2011, Lahmar et al., 2012, Kumar et al., 2016), clearly indicative of positive increase in the infection with age. Old animals are likely to acquire infection, possibly due to their longer exposure to infection and lower immunity to combat infection. Out of these 12 cases, 6 animals were non-pregnant and 6 were pregnant. Equal prevalence of infection has been reported in breeding and non-breeding populations (Singh et al., 2014). Khan et al. (2010) reported higher prevalence in female animals as compared to males. The most likely reason is that female animals are kept for a longer period of time due to production reasons and also immunodeficiency and decreased cell-mediated immunity in pregnancy and the lactation period may increase the susceptibility of females for cystic infection (Pour et al., 2012). Four animals were anorexic with rest of the animals having partial anorexia. Kumar et al. (2016) reported partial anorexia in 38% and rest 62% were completely anorectic. The physical examination parameters were within the normal range except for respiration rate >50 in two buffaloes and one cattle. Cardiac auscultation revealed tachycardia (HR >100 bpm) in three cattle. Three buffaloes had muffled heart sounds, otherwise all other animals had normal intensity of heart sounds. Tachycardia and muffled heart sounds are the pathognomic indicators of congestive heart failure but have also been reported in cases with thoracic lesions (abscess or tumours) (Abdelaal et al., 2009).
The clinical signs that increased the suspicion of cardiac involvement are depicted in Table 1. The cited literature reports hydatid disease is asymptomatic in the intermediate host (Jayathilakan et al., 2010). However, the spectrum of clinical signs may vary and depend on the number, size, severity of cystic lesions and adjacent organs, resulting in impaired function of that particular organ (Besbes et al., 2010). Apart from loss of defecation and tympany, Kumar et al. (2016) reported brisket edema in 11.11% and respiratory distress in 31.11% bovines with lung and/or liver cysts, which is far less than observed in the present study.
Table 1: Clinical signs in bovines with lung and/or liver cysts (n=12)
|Clinical Signs||Buffalo (n=7)||Cattle (n=5)||Total (n=12)|
|Bilateral jugular engorgment||2(28.6%)||1(20%)||3(25%)|
|Dyspnoea/open mouth breathing||3(42.8%)||3(60%)||6(50%)|
|Abduction of elbows||2(28.6%)||1(20%)||3(25%)|
In a recent study, Chuadhari et al. (2017) reported coughing, dyspnoea and stridor in three dairy animals with cystic echinococcosis in the lung parenchyma. Respiratory distress or open mouth breathing in the present study could be correlated with the location and size of cysts present in the lung parenchyma leading to reduced functional space of the lung (Besbes et al., 2010). Presence of cystic densities in the pleural cavity may have lead to the development of edema of the ventral parts of the body and bilateral jugular engorgement. Tumours, abscesses, echinococcus cysts, swollen lymph nodes have been reported to cause pseudopericarditis in bovines with similar signs like neck edema and jugular vein engorgement (Keles et al., 2003). The jugular veins can be distended, without signs of right-sided cardiac insufficiency due to obstruction or compression of the cranial vena cava by thrombi or intrathoracic masses (Braun et al., 2007).
Hematological findings viz. haemoglobin 9.67±0.56 g% (Mean±SE) and total leukocyte count 8793.33±925.26/μl (Mean±SE). All the 12 animals had a normal hemogram except for anemia in two cases. Chaudhari et al. (2017) reported haemoglobin to be 8.6 ± 4.20 g/dl and total leukocyte count-10,605 ± 3904.89/μl in three dairy animals with cystic echinococcosis presented with signs of coughing, dyspnoea and stridor. The mean values of various biochemical parameters from the present study are given in Table 2. In the current study the values of liver function tests (AST and GGT) were higher than the normal physiological reference range (Radostits et al., 2007). The increase in the liver enzyme values can be attributed to dysfunction of the organ caused by the presence of cysts which may have ultimately lead to passive liver congestion thus appearance of symptoms like that of congestive heart failure viz. brisket edema and jugular engorgement. Serum total protein and albumin levels in the present study were also lower than the reference range for healthy animals (Radostits et al., 2007). The results can be ascribed to chronic anorexia (Kaneko, 1997) or failure of liver to synthesize adequate amounts of protein due to impaired liver function (Tennant and Center, 2008). Significantly decreased levels of serum albumin and creatinine have been reported in sheep with cystic echinococcosis (Sagkan-Ozturk et al., 2015). However, in the present study the values of serum BUN and creatinine were within the normal range. It has been previously reported that cystic echinococcosis grows progressively and produces pressure atrophy in the affected organs, leading to functional alterations (Barnes et al., 2011).
Table 2: Mean±SEM of various biochemical parameters in animals with liver and/or lung disease (n=12)
|Parameter||Buffalo (n=7)||Cattle (n=5)||Overall (n=12)|
1Values are Mean±SEM of that particular parameter; 2Values in parenthesis depict range
Ultrasonography efficiently aided in the detection of single or multiple, encapsulated, thin or thick walled cavitary lesions, within the hepatic parenchyma (Fig. 1) in 83.33% cases and lung tissue (Fig. 2) in 91.66% of the presented animals. Tolosa et al. (2009) reported highest prevalence of cysts in lungs (57%) followed by liver (34%), spleen (5%), heart (3%) and kidneys (1%). Our findings are in co-relation with Nadery et al. (2011), Pour et al. (2012) and Khan et al. (2013) who also reported higher prevalence in lungs as compared to liver. In the current study no cysts were detected in the heart upon ultrasonography. Similar results were reported by Khan et al. (2013) in an abbatoir study of hydatidosis in buffaloes. Nine out of twelve animals (75%) had both lung and liver cysts on ultrasonography, suggestive of high co-occurrence of lung and liver cysts in the intermediate host. Kumar et al. (2016) reported concurrent infection of both hepatic and pulmonary parenchyma in 46.7% of the animals. In our study more number of animals were found to be affected with multiple cysts of lung (n=8) and liver (n=7) (Table 3). The probable explanation of this finding could be the long course of illness as most of the animals presented to us were sick from nearly one month. Clinical manifestations are mild in the early stage, which can be overlooked by the owner, while as the cysts gradually grow and multiply, the parasite may physically damage tissues and organs, which can become dysfunctional at the later stages of echinococcosis and thus leads to appearance of severe signs (Zhang and Mc Manus, 2006).
Table 3: Ultrasonographic detection of single or multiple cysts in liver and/or lung
|Number of Cysts||Single Cysts||Total||Multiple Cysts||Total||Grand Total|
|Lung (n=11)||1||2||3 (27.3%)||6||2||8 (72.3%)||11|
|Liver (n=10)||1||2||3 (30%)||5||2||7 (70%)||10|
After the diagnosis of lung and/or liver cyst was made, a further evaluation about the effect of cystic density in the affected organ and the adjacent organ structures was attempted. Among buffaloes, two animals had pleural effusions but these were without any signs of respiratory distress or dyspnoea (Table 4).
Table 4: Ultrasonographic detection of other conditions due to presence of cysts in lung and/or liver (n=12)
|No.||Clinical SIGNS||No.||Clinical Signs|
|Pleural effusions (n=2)||2||Brisket edema (1), Brisket+limb+jowl edema (1)||0||–|
|Hepatic congestion (n=8)||4||Brisket edema (4), jugular engorgment (2), dyspnoea (2)||4||Brisket edema (2), dyspnoea (2)|
|Compression of heart (n=8)||5||Brisket edema (5), jugular engorgement (2), dyspnoea (2)||3||Brisket edema (1), dyspnoea (2)|
Dyspnoea or open mouth breathing, in this study, could be correlated to the size, location or severity of cystic lesions in the lung parenchyma (Besbes et al., 2010). USG of four buffaloes and four cows having brisket edema and jugular engorgement also showed marked hepatic congestion characterized by dilated and oval or round caudal vena cava (Fig. 3). Persistent dilatation of posterior vena cava is indicative of systemic congestion. It may be caused by cardiac insufficiency due to pericarditis, thrombosis of the caudal vena cava or compression of the caudal vena cava in the thorax or in the subphrenic region by some space-occupying lesion (Kumar et al., 2012). An interesting finding in the present study was the acute compression of heart (buffaloes-5, cattle-3) due to massive cystic degeneration of the lungs leading to cardiac tamponade wherein heart is unable to pump blood to its full capacity (Fig. 4).
|Fig. 3: Ultrasonographic image of liver showing hepatic congestion (dilated caudal vena cava (CVC) and hepatic veins (HV)||Fig 4: Cardiac ultrasound image showing compression of the heart due to multiple cystic densities (C). Left ventricle (LV), Right ventricle (RV)|
The cardiac ultrasound in these cases revealed diastolic compression of the ventricles, findings typical in cardiac tamponade (Firshman et al., 2006). Otherwise the heart appeared to be normal with no pericardial deposits/effusions, thus confirming the cysts to be the primary cause of clinical symptoms mimicking signs of congestive heart failure in the animals included in the current study.
Depending on the number, size and location, lung and/or liver cysts can be the primary cause of disease. Ultrasonography could be used as a screening tool in living animals for the detection of lung and/or liver cysts in the endemic areas to prevent the spread of this disasterous zoonoses. Hydatid disease still remains an asymptomatic disease in the intermediate hosts and veterinarians should consider this disease for differential diagnosis while investigating the cause of clinical signs like brisket edema, jugular engorgement and dyspnoea etc.